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Conservation biology of the European pond turtle Emys orbicularis (L) in Italy M.A.L. ZUFFI Abstract Key words The updated situation and knowledge Emys orbicularis, distribution, ecology, of the biology, ecology, behaviour and pro- conservation, Italy, tection of the European pond turtle, Emys orbicularis (L.) in Italy is presented and discussed in the light of conservation bio- logical issues. Stapfia 69, zugleich Kataloge des OÖ. Landesmuseums, Neue Folge Nr. 149 (2000), 219-228 219 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Conservation biology of the European pond turtle Emys ... · Conservation biology of the European pond turtle Emys orbicularis (L) in Italy M.A.L. ZUFFI Abstract Key words The updated

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Conservation biology of the Europeanpond turtle Emys orbicularis (L)in Italy

M . A . L . Z U F F I

Abstract Key words

The updated situation and knowledge Emys orbicularis, distribution, ecology,

of the biology, ecology, behaviour and pro- conservation, Italy,

tection of the European pond turtle, Emys

orbicularis (L.) in Italy is presented and

discussed in the light of conservation bio-

logical issues.

Stapfia 69,zugleich Kataloge des OÖ. Landesmuseums,Neue Folge Nr. 149 (2000), 219-228

219

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Introduction

Populations of Emys orbicularis in Italy are

distributed mainly in coastal areas and inter-

nal plains. Most regions of Italy have been

mapped, but in some cases the information is

incomplete (Fig. 1, Societas Herpetologica

Italica 1996). An uncomplete knowledge of

habitat use leads to a biased view on the

Fig. 1:The actual distribution of f. orbicularisin Italy (Societas Herpetologica Italica1996).

autecology of a species. This fact must be

carefully considered when data on the distri-

bution aid to protect or manage a given species.

For the European pond turtle in Italy,

several studies have been conducted since the

beginning oi the nineties, and until recently,

this species was relatively unknown from a

scientific point of view (LANZA 1983).

In this last decade, a "Big Bang" of interest

in Italian populations of E. orbiculans enabled

to build up a consistent data set. Information

on biometry (Zum & GARIBOLDI 1995a, b),

systematics (FRITZ & OBST 1995; FRITZ 1998),

population structure (KELLER et al. 1998; KEL-

LER 1999), space usage (LEBBOROM & CHELA -

ZZI 1991), reproductive biology (ZUFFI &

ODETTI 1998; ZUFFI et al. 1999; KELLER 1999),

and thermal ecology (Dl TRAM & ZUFFI

1997), have become available. However, only

a few studies have focused on the conservati-

on biology of E. orbicularis in Italy (GARIBOL-

OI & ZUFFI 1994; LEBBORONI &. CHELAZZI

1998; CHELAZZI, LEBBORONI, TRIPEPI, UTZERI

& ZLFFI 1999).

On the basis of colouration, markings,

body size and shape of E. orbicularis specimens

throughout the distribution range, several

morphological subspecies have been recogni-

zed, some of which have also been confirmed

by a genetical approach (LENK et al. 1998;

FRITZ & OBST 1995; ODETTI, MANCINO, BATI-

STONI & ZUFFI 1999; Zum et al. unpubl.). Pri-

or to this, subspecies have not been conside-

red. It is consequently of great importance to

conduct any future studies with taking the

subspecies' identity into account.

Conservation biology is a relatively young

working field. Projects should incorporate all

known aspects of the target species, and it

should be structured as an open, changeable

and integrable framework.

This contribution is based on recent work

on E. orbiculans in Italy, with a particular

emphasis on interdisciplinary approaches

(e.g. ecology-, ethology and genetics). The aim

is to present results from Italian populations

and to stimulate an interdisciplinary discussi-

on on the biology of E. orbicularis in southern

European countries. The following aspects are

considered as basic for conservation biological

aspects of the European pond turtle:

i) distribution patterns and population

status,

ii) habitat use,

lii) reproductive behaviour,

iv) reproductive biology and

v) nest predation.

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Materials and methods Results

I considered data from unpublished thesis

of my research team (Dl TRAM 1989; OPETTI

1997; FABBRI 1999; ROVINA 1999), and

recently published work (LEBBORONI &. CHE-

LAZZI 1991; MAZZOTTI 1995; ZUFFI & GARI-

BOLDI 1995a, 1995b; ROVERO & CHELAZZI

1996; Di TRANI & Zum 1997; LEBBOROM &

Distribution patterns and popula-tion status

The subspecies E. o. galloitalica is found

along the Ligurian and the Thyrrhenian coasts

southwards to the Gulf of Policastro and is

also present in Sardinia and Corsica. Em\s o.

cf. hellenica occurs in southern Italy, while the

CHELAZZI 1998; Zum & ODETTI 1998; ZUFFI,

ODETTI & MEOZZI 1999). Generally, each cap-

tured specimen was measured and weighed,

and marked with individual plastic tags on the

carapace (Fig. 2) and permanent notches on

the marginal scutes. The reproductive status

of adult females was determined with inguinal

palpation and the count of oviductal eggs with

radiographs. Clutch size was determined by

counting eggs from intact nests.

Variables were generally tested under nor-

mality and statistical analyses were performed

with parametric or non-parametric methods.

For further details, it is suggested to follow the

original paper.

taxonomy of populations from the Padane

plain is still uncertain (FRITZ &. OBST 1995;

LENK, JOGER, FRITZ, HEIORICH & WINK 1998).

The European pond turtle is mainly distribu-

ted along the coasts and areas at low elevation

and occurs sporadically in several areas in north-

western Italy (Societas Herpetologica Italica

1996). Most of the largest Italian populations

are found in nature parks, biological reserves,

and protected areas (LEBBORONI &. CHELAZZI

1991; GARIBOLDI & Zum 1994; ZUFFI &

GARIBOLDI 1995; RAVAGU 1996; ROVERO &

CHELAZZI 1996; UTZERI et al. 1996; Zum et al.

1999). None of these populations seems to be

at risk of extinction, but this conclusion might

be caused by a lack of knowledge. Habitat

Fig. 2:Each captured specimen was markedwith plastic tags on the carapace andwith permanent notches on the margi-nal scutes.

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changes caused by human activities, also in

protected areas, is a relatively recent pheno-

menon. The negative consequences for E.

orbicularis remain to be shown. Some relictual

and small populations in the central and

western parts of the Po plain (northern Italy)

are believed to be endangered (GARIBOLDI &

Zum 1994). The low number of reported hat-

chlings and juveniles in some of these areas

Fig. 3:The "canal" habitat is characterised byartificial drainage canals and open ormarginal areas (Bosco Mesola).

could be due to a lack of data, and in some

areas it is very difficult to find nests, even if

juveniles are abundant. Younger age-classes

are often underestimated, in comparison with

the older classes, both due to lower detectabi-

lity and different habitat use (see below).

Supposed competition between Emys orbi-

cularis and the various subspecies of Trachemys

scripta actively or accidentaly introduced into

natural and artificial ponds and wetlands in

Italy has yet to be demonstrated (LuiSELLl,

CAPLLA, CAPIZZI, FIUPPI, TRUJILLO JESUS &

ANIBALDI 1997).

The effective protection of wild populati-

ons by habitat protection and the limitation of

animal trade is afforded by the Bern Conven-

tion (1979) and Washington Convention

(1980), the latter better known as CITES.

Other effective measures are found in the

local legislation of Natural or Regional Parks

and Reserves, which have included the Euro-

pean pond turtle among protected species or

which protect all living organisms in the

reserve.

Habitat use

Populations of E. orbicularis in Italy are

mainly found in two different kinds of habitat,

the former being represented by "pond"

systems, consisting of one or more natural,

shallow water bodies, generally in forest areas

(Monte Rufeno, Pollino, Castel Poniano),

and the latter being the "canal" habitat (Bos-

co Mesola (Fig. 3), Uccellina, Tombolo) (L.EB-

BOROM & CHELAZZI 1998), which is characte-

rised by artificial drainage canals, generally in

open or marginal areas. During a long-term

study in the "Monte Rufeno" Natural Reserve

(northern Latium, central Italy), LEBBORONI

& CHELAZZI (1998) found that the population

o( E. orbicularis is sub-divided into different

groups, each oi which tied to a distinct pond

system, with no consistent exchange of turtles

from one system to another. Each of the pond

systems includes a permanent primary pond

where most adult turtles spend the entire year,

and a number of satellite ponds of different

types (temporary primary ponds, permanent

secondary ponds, and temporary secondary

ponds). In the Tombolo area (S. Rossore Fig.

4.. Camp Darby) there are both habitat types.

Canals are permanently flooded and overland

movements are rare. Canals are inhabited by

the same individuals over the whole year.

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Reproductive behaviour

Overland movements for nesting differamong populations depending on the locationof suitable nesting areas. In canal systems(Bosco Mesola, Tombolo, Uccellina) nests aregenerally dug in open sunny areas, with lowdensity vegetation, 2 to 20 m from the river'sbank (ODETTI 1997; ROVINA 1999; Zum &

GARIBOLDI unpubl.). Females usually lay3-9 eggs (mode 6) in nests of about 6-8 cm indiameter and 5-10 cm deep (e.g., Dl TRANI1989: n=78; ROVINA 1999: n=209; Zum &GARIBOLDI unpubl. data: n=75). In forest areasa large fraction of females may migrate up to1000 m from their pond systems for nesting(ROVERO &. CHELAZZ1 1996), which generallyoccurs in the first hours of night. Then females return to their home ponds, after a periodvarying from 36 hours to one week, dependingon weather conditions and/or distance of thenesting sites. The start of the nesting migrati-on is related to the increase of average air tem-perature (MARANGIO 1999). Suitable nestingareas are bushy, sunny clearings with marly-limestone soil, situated on slopes or at the baseof small landslides. All females inhabiting thesame pond system were recorded to lay eggswithin the same nesting area year after year.During nesting migration females spend dayti-me in permanent secondary ponds (Fig. 5),where they pump water for softening the soilduring digging into the accessory urinary blad-der. At sunset they start searching for a speci-fic nest site, generally under a shrub (Juniperus

communis), in grass, or next to a stone, prefe-rably on a gentle slope with an east to sout-hwest exposure. Sometimes females dig sever-al holes before laying. In the Pisa population50% of total nests (n=209 nests) were within6 m from the water's edge, and 90% within 20m. Frequency of nests was significantly higherin North to South canals with respect to tho-se oriented East to West (152 vs 57 nests, X '

= 144.17, 1 df, P < 0.001; ROVINA 1999).Vegetation probably limits direct exposure ofnests to the sun. In most cases there is a strongcorrelation between nest locations and theirrelative distance from surrounding vegetation.

Incubation lasts between 80 and 90 days,and the hatching coincides with the autumnalflooding of the temporary secondary ponds(Fig. 6). Hatchlings probably spend their firstyear in other habitats than the adult population.

In the Monte Rufeno population, hatchlings

(average carapace length 24 mm, weight 3.7 g,

n=18) inhabit small temporary ponds of

1-5 m-, 5 to 40 cm in depth. In a few cases

hatchlings were recorded to overwinter in

their nest and emerged in the following

spring, as observed also in Tuscanian populati-

ons (Zum 1995 unpubl. data; OPETTI 1997,

unpublished thesis, University of Pisa).

Fig. 4:Each of the pond systems includes apermanent primary pond where mostadult turtles spend their entire year(San Rossore).

Fig. 5:During nesting migration femalesspend daytime in permanent secon-dary ponds, where they pump waterinto the accessory urinary bladder(f. o. galloitalica).

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Reproductive biology

The reproductive patterns of Italian popu-

lations are summarized in Tab. 1. In E. orbicu-

laris the frequency of egg production varies

with latitude, with the northernmost popula-

tions generally laying larger clutches (MlTRUS

& ZEMANEK 1998; KELLER 1999), and the sou-

thernmost laying a small clutch (Zum &

Fig. 6:A hatchingjuvenile ofSan Rossore:hatching iscoinciding withthe autumnalflooding.

Table 1 - Reproductive parameters of E. orbicularis in Italy. CL = mean carapace lengthof reproductive females; SD = standard deviation; n.r.=not recorded. Reproductive fre-quency = mean percentage of reproductive females nesting yearly. CS = mean clutchsize (from CHELAZZI et al., 1999)

Localities

a (so)Cm

Reproductive

frequency

CS(SD)

Bosco

Mesola

13.63(1.14)

N=50

n.r.

Tombikj Uccellina M.Rufeno C.Porziano Pollirto

13.17(0.97) 12.52(0.88) 12.12(0.76) 13.43(1.23) n x

N=115 N=41 N=18 N=34

20-58.3% 80-85% 32.5%

5.08 (0.30) 5.91 (0.23) 3.70 (0.82)

N=15 N=18 : N=10n.r.

Clutch

frequency

Egg deposition

Nest predation

Activity

Latitude

Alt. (m a.s.1.)

Mediterrane

an basin

Subspecies

Source

1 1-2 1-2 1-2

May-July

8 5 «

March-October

44.55

Jtoy-July

75%

May-July June nx75% 90%

February- March- March-

November October October

43.40 42.40 42.45

55010

nx

nx nxMarch- mid March-

October mid October

41.40 39.19

10 1000

EAST WEST WEST WEST WEST EAST

orbicularis galloitalka galloitalica galloitalica galloitalica hellenka

ZUFFI &

GARIBOLDI,

ZUFFI &

1998;ZUFFI

etal.. 1999

DITRANI

1989;

Di TRAM &

Zum. 1997;

ZUFFI,

ROVERO &

CHELAZ2

1996;

LEBBORONI

& CHELAZZI,

UTZERI

etal..

unpubl.

data

TRIPERI

etal..

unpubl.

data

unpubl. data 1998

ODETTI, 1998). In the Italian populations,

reproductive females ranged from 69.2 to

100% of the total adult female sample (ZUFFI

& ODETTI 1998; ROYIN A 1999; LEBBORONI et

al. unpubl. data). For the first time in the

European pond turtle, a double egg laying was

recorded in at least two Tyrrhenian populati-

ons (Tuscany: ZUFT-I &. ODETTI 1998; Latium:

SERRA, 1998), but we cannot determine the

frequency of such occurrences (ODETTI 1997,

Zum & ODETTI 1998, ROVINA 1999). The

estimated presence of oviductal eggs (Zum &

ODETTI 1998) is about 39 ± 6 days (n=15) and

the time between two consecutive periods

with detectable oviductal eggs is about 9-11

days. Although clutch frequency is the most

important parameter for studies on turtle

reproductive biology (GIBBONS et al. 1982),

the occurrence of double egg deposition is pro-

bably subject to underestimation. However,

estimation based on the Tuscanian populati-

on, indicated that from 2.3 to 70.8% of the

reproductive females may lay eggs twice a year

(ODETTI 1997, Zum & ODETTI 1998; ROVINA

1999).

Nest predation

A marked predation oi nests, with estima-

ted values of about 75% was recorded at

almost all of the sites (Di TRANI 1989, n = 89

nests; Zum et al. 1999, n = 33 nests; ROVINA

1999). Possible nest predators, among mam-

mals, are the badger (Meles meles), the wild

boar (Sus scrofa), the red fox (Yulpes iiilpes),

the common rat (Rattus rauus), the wood

mouse (Apodemus sykaacus), and the nort-

hern water vole (Murrotus urrestns). and,

among birds, the jay (Garruius $andanus).

Damage occurs by large mammals, for example

wild boar and fallow deer, which walk on the

soft ground around temporary or permanent

ponds. Also humans, for example military per-

sonnel or guardians of protected areas, may

occasionally break freshly dug nests or kill hat-

chlings around wet areas. In the Migliarino, S.

Rossore, Massaciuccoli natural park (Nort-

hern Tuscany), a damage to canal borders by

farm tractors passing too close to nesting areas

during reproductive season (pers. observ.) or

when cutting reeds during winter or early

spring has been noted.

224

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In all studied sites, protection of nests by

means of wire-net cages and fences proved

very effective in raising nest survival to 95-

100% (n = 20; ODETTI 1997), with respect to

natural predators.

Discussion

The basic data set so far is not surprisingly

linked to a common situation: scientific

activities are carried out in natural areas adja-

cent to university and museums. In Italy this

seems to be the case for E. orbicularis, and the

lack of research (Societas Herpetologica Itali-

ca 1996) is due to the absence of experts.

The inventory, study and awareness ofavailable natural resources leads to a betterunderstanding of all biological variables,necessary for the management and conservati-on of species. In the USA, after decades oflong-term studies across a wide range of inte-rests, it is now possible to better understandthe phenotypic plasticity of wild populationsof some species of terrapins and land tortoises(among others ELGAR & HEAPHY 1989; IVER-SON et al 1993; ROWE 1994).

Further studies on E. orbicularis are needed for

the understanding of

1) latitudinal and altitudinal trends in repro-ductive patterns;

2) the influence of habitat features on repro-ductive success;

3) determine the reproductive parametersresponsible for long-term populationdynamics;

4) human pressure.

Finally I suggest that a conservation biolo-

gy and management plan for E. orbicularis

should cover:

a) the understanding of the taxonomic statusby means of morphological and molecularmethods;

b) the identification of the habitats requiredby different age-classes all around the year;

c) consideration of migration routes andmovement patterns of reproductive andpost reproductive females;

d) protection of nests against predation andthe limitation of human activities in, orclose to, nesting areas;

e) the limitation or interruption of intro-duction projects in non-protected environ-ments;

0 the ecosystem reconstruction and (sub)spe-cies reintroduction in areas previouslyinhabited by E. orbicularis;

g) quantitative and/or qualitative projectsregarding introduction, reintroduction,population reinforcement or populationmanagement into protected areas, inorder to verify the suitability of the propo-sed methods.

Acknowledgements

I am pleased to thank very much all friends

and colleagues who in various ways have

helped me towards the preparation of this con-

tribution. In particular, I wish to express my

special gratitude to my field co-workers Drs.

Maria Elena FABBRI, Francesca ODETTI, Laura

ROVINA, and to Miss Francesca Dl BENEDETTO,

(Museum Natural History, University of Pisa)

and to Dr. Corinne Dl TRANI (Moulhouse Zoo-

logical Garden); to my colleagues Dr. Renata

BATISTONI and Prof. Giorgio MANCINO (Dept.

Cellular Biology, University of Pisa) for lab

facilities; to Prof. Carlo UTZERI (Dept. Animal

and Human Biology, University of Rome "La

Sapienza") and Sandro TRIPEPI (Dept. Animal

Ecology, University of Calabria). Dr. Claudia

CORTI and Marta POGGESl for permission to

study the Herpetological Collection at "La Spe-

cola" Zoological Museum (University of Flo-

rence). Last but not least, I thank Dr. Marco

LEBBORONI (Dept. Animal Biology and Gene-

tics, University of Florence) for the continuous

exchange of ideas and comments.

This work was partly financed with

MURST funds to Prof. Franco STRUMIA

(Director, Museo di Storia Naturale e del Terri-

torio, University of Pisa).

Zusammenfassung

Die gegenwärtige Situation und der Kennt-

nisstand von Biologie, Ökologie und Verhalten

der Europäischen Sumpfschildkröte in Italien

wird unter dem Aspekt des Artenschutzes

beschrieben und diskutiert.

225

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Anschrift des Verfassers:

Dr. Marco A.L. ZUFFlCurator of Zoology ComparativeAnatomyMuseo di Storia Naturale e delTenitorio, Universita di PisaVia Roma 79, 56011Calci (Pisa)Italye-mail:[email protected]

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